The molecular mechanisms of rapid thermal adaptation in European grayling

Adaptation is a key evolutionary process which may be important to maintain population viability during rapid environmental changes. The European grayling (Thymallus thymallus) is a freshwater salmonid that effectively colonises new environments despite low genetic diversity. Several new grayling populations were recently established from a single ancestral gene pool in a Norwegian water system. Phenotypic responses to colder or warmer temperature (thermal origin) during spawning and early development have been reported but the molecular mechanisms underlying these changes are often poorly understood. The aim of this thesis was to investigate the molecular mechanisms of thermal adaptation in this Norwegian grayling system using multi-omics approaches. A prior common-garden experiment, where embryos from several populations from warmer and colder thermal origins were reared in higher and lower tempearatures, was utilised. (I) RNA-sequencing study of the common-garden populations revealed that the gene expression response was mostly plastic (to rearing temperature) but an adaptive signal (to thermal origin) existed in specific gene modules. (II) A hybrid synteny-guided chromosome-level genome assembly confirmed that graylings have a unique chromosomal setup among salmonids, with the karyotypes having evolved through pericentric inversions and one chromosomal fission rather than multiple fusions, which are typical to other salmonids.. It also revealed a similarly distinctive transposable element content in comparison to Atlantic salmon (Salmo salar). (III) Whole-genome cytosine sequencing of the common-garden populations uncovered common methylation patterns among populations from similar thermal origins, and almost absent plasticity. (IV) A whole-genome population genomics study revealed candidate SNP loci for thermal adaptation. Biological processes associated with thermal origin overlapped between the molecular levels. The results describe how rapid thermal adaptation may be manifested by altering standing genetic variation and epigenetic variation. They highlight the value of applying “omic” methodologies when studying adaptive biodiversity e.g. for fisheries management and conservation applications.--- Adaptaatio on evoluution avainprosessi, joka voi olla tärkeä populaation elinkelpoisuuden säilymiseksi nopeiden ympäristönmuutosten aikana. Harjus (Thymallus thymallus) on makean veden lohikala joka kolonisoi tehokkaasti uusia ympärisöjä matalasta geneettisestä diversiteetistä huolimatta. Useita uusia harjuspopulaatioita syntyi nopeasti yhdestä geenipoolista norjalaisessa vesistöjärjestelmässä. Fenotyyppisiä vasteita kylmempään tai lämpimämpään lämpötilaan (alkuperäislämpötila) kudun ja aikaisen kehityksen aikana on raportoitu, mutta niiden taustalla olevat molekyylimekanismit ovat huonosti ymmärrettyjä. Tämän väitöskirjan aiheena oli tutkia lämpöadaptaation molekyylimekanismeja tässä norjalaisessa systeemissä käyttämällä montaa eri “omics”-lähestymistapaa. Tutkimuksessa käytettiin hyväksi aiempaa yhteispuutarhakoetta, jossa kasvatettiin useista suhteellisen lämpimään ja kylmään lämpötilaan adaptoituneista populaatioista peräisin olevia alkioita lämpimämmissä ja matalammissa lämpötiloissa. (I) Yhteispuutarhapopulaatioiden RNA-sekvensointi paljasti, että geeniekspressio oli pääosin plastista (vastasi kasvatuslämpötilaan) mutta adaptiivinen signaali (vaste alkuperäislämpötilaan) löytyi tietyistä geenimoduleista. (II) Harjuksen genomisekvenssi selvitettiin koromosomitasolle synteniaa hyödyntävän hybridimenetelmän avulla. Se vahvisti, että harjuksen uniikki kromosomisto on kehittynyt kromosomien perisentristen inversioiden ja yhden fission, eikä lohikaloille tyypillisten kromosomifuusioiden, seurauksena. Myös atlantinlohesta (Salmo salar) poikkeava liikkuvien elementtien kokoonpano havaittiin. (III) Yhteispuutarhakoepopulaatioiden genomien sytosiinisekvensointi paljasti yhteneviä epigeneettisiä markkeriyhdistelmiä samankaltaisista alkuperäislämpötiloista peräisin olevissa populaatioissa, ja lähes puuttuvan plastisuuden. (IV) Koko genomin populaatiogenomiikkakokeessa havaittiin lämpötila-adaptaation kandidaattilokuksia. Alkuperäislämpötilaan liittyvät biologiset prosessit olivat osittain samoja eri molekyylitasojen välillä. Tulokset selventävät miten nopea lämpöadaptaatio voi seurata olemassaolevan geneettisen muuntelun ja epigeneettisen muuntelun kautta, ja korostavat “omics”-lähestymistapojen arvoa adaptiivisen biodiversiteetin tutkimisessa mm. kalakantojen ja muiden lajien suojelemiseksi

Modularity Facilitates Flexible Tuning of Plastic and Evolutionary Gene Expression Responses during Early Divergence

Gene expression changes have been recognized as important drivers of adaptation to changing environmental conditions. Little is known about the relative roles of plastic and evolutionary responses in complex gene expression networks during the early stages of divergence. Large gene expression data sets coupled with in silico methods for identifying coexpressed modules now enable systems genetics approaches also in nonmodel species for better understanding of gene expression responses during early divergence. Here, we combined gene coexpression analyses with population genetics to separate plastic and population (evolutionary) effects in expression networks using small salmonid populations as a model system. We show that plastic and population effects were highly variable among the six identified modules and that the plastic effects explained larger proportion of the total eigengene expression than population effects. A more detailed analysis of the population effects using a QST - FST comparison across 16,622 annotated transcripts revealed that gene expression followed neutral expectations within modules and at the global level. Furthermore, two modules showed enrichment for genes coding for early developmental traits that have been previously identified as important phenotypic traits in thermal responses in the same model system indicating that coexpression analysis can capture expression patterns underlying ecologically important traits. We suggest that module-specific responses may facilitate the flexible tuning of expression levels to local thermal conditions. Overall, our study indicates that plasticity and neutral evolution are the main drivers of gene expression variance in the early stages of thermal adaptation in this system.Peer reviewe

Population connectivity predicts vulnerability to white-nose syndrome in the Chilean myotis (Myotis chiloensis) - A genomics approach

Despite its peculiar distribution, the biology of the southernmost bat species in the world, the Chilean myotis (Myotis chiloensis), has garnered little attention so far. The species has a north-south distribution of c. 2800 km, mostly on the eastern side of the Andes mountain range. Use of extended torpor occurs in the southernmost portion of the range, putting the species at risk of bat white-nose syndrome, a fungal disease responsible for massive population declines in North American bats. Here, we examined how geographic distance and topology would be reflected in the population structure of M. chiloensis along the majority of its range using a double digestion RAD-seq method. We sampled 66 individuals across the species range and discovered pronounced isolation-by-distance. Furthermore, and surprisingly, we found higher degrees of heterozygosity in the southernmost populations compared to the north. A coalescence analysis revealed that our populations may still not have reached secondary contact after the Last Glacial Maximum. As for the potential spread of pathogens, such as the fungus causing WNS, connectivity among populations was noticeably low, especially between the southern hibernatory populations in the Magallanes and Tierra del Fuego, and more northerly populations. This suggests the probability of geographic spread of the disease from the north through bat-to-bat contact to susceptible populations is low. The study presents a rare case of defined population structure in a bat species and warrants further research on the underlying factors contributing to this. See the graphical abstract here.Peer reviewe

Genetic-based evaluation of management units for sustainable vendace (Coregonus albula) fisheries in a large lake system

The goal of the processing industry, trade and consumers is to get eco-labelled freshwater fish products from sustainable fisheries into the market as soon as possible. The fourth largest natural lake system in Europe, the Saimaa lake system supports a fishery for vendace (Coregonus albula). Certification of the fishery requires an understanding of population structure to help determine the number and spatial extent of management units. In this study, we analysed the genetic diversity of local vendace populations in the Saimaa lake system and aimed to identify the conservation and management units of vendace. Within the Saimaa, the genetic divergence between local populations of vendace was weak and their genetic divergence did not follow an isolation by geographic distance pattern. Vendace has potential to disperse effectively within and between local populations in different lake basins. Even if we observed subtle genetic divergence within our study systems, available information showed no significant evidence that the local populations had unique evolutionarily significant traits. The local populations of the Saimaa lake system seem to have similar life history and morphological traits as in the whole Central Finland lake district. The conservation of genetic diversity seemed not to require basin-specific actions and we conclude that management of local vendace populations of Saimaa as one management unit is advisable

Population Connectivity Predicts Vulnerability to White-Nose Syndrome in the Chilean Myotis (Myotis chiloensis)-A Genomics Approach

Despite its peculiar distribution, the biology of the southernmost bat species in the world, the Chilean myotis (Myotis chiloensis), has garnered little attention so far. The species has a north-south distribution of c. 2800 km, mostly on the eastern side of the Andes mountain range. Use of extended torpor occurs in the southernmost portion of the range, putting the species at risk of bat white-nose syndrome, a fungal disease responsible for massive population declines in North American bats. Here, we examined how geographic distance and topology would be reflected in the population structure of M. chiloensis along the majority of its range using a double digestion RAD-seq method. We sampled 66 individuals across the species range and discovered pronounced isolation-by-distance. Furthermore, and surprisingly, we found higher degrees of heterozygosity in the southernmost populations compared to the north. A coalescence analysis revealed that our populations may still not have reached secondary contact after the Last Glacial Maximum. As for the potential spread of pathogens, such as the fungus causing WNS, connectivity among populations was noticeably low, especially between the southern hibernatory populations in the Magallanes and Tierra del Fuego, and more northerly populations. This suggests the probability of geographic spread of the disease from the north through bat-to-bat contact to susceptible populations is low. The study presents a rare case of defined population structure in a bat species and warrants further research on the underlying factors contributing to this. See the graphical abstract here

Genetic-based evaluation of management units for sustainable vendace (Coregonus albula) fisheries in a large lake system

The goal of the processing industry, trade and consumers is to get eco-labelled freshwater fish products from sustainable fisheries into the market as soon as possible. The fourth largest natural lake system in Europe, the Saimaa lake system supports a fishery for vendace (Coregonus albula). Certification of the fishery requires an understanding of population structure to help determine the number and spatial extent of management units. In this study, we analysed the genetic diversity of local vendace populations in the Saimaa lake system and aimed to identify the conservation and management units of vendace. Within the Saimaa, the genetic divergence between local populations of vendace was weak and their genetic divergence did not follow an isolation by geographic distance pattern. Vendace has potential to disperse effectively within and between local populations in different lake basins. Even if we observed subtle genetic divergence within our study systems, available information showed no significant evidence that the local populations had unique evolutionarily significant traits. The local populations of the Saimaa lake system seem to have similar life history and morphological traits as in the whole Central Finland lake district. The conservation of genetic diversity seemed not to require basin-specific actions and we conclude that management of local vendace populations of Saimaa as one management unit is advisable.peerReviewe

Whole-genome analysis reveals contrasting relationships among nuclear and mitochondrial genomes between three sympatric bat species

Understanding mechanisms involved in speciation can be challenging, especially when hybridization or introgression blurs species boundaries. In bats resolving relationships of some closely related groups has proven difficult due subtle interspecific variation both in morphometrics and molecular datasets. The endemic South American Histiotus bats, currently considered a sub-genus of Eptesicus, harbor unresolved phylogenetic relationships and of those is a trio consisting of two closely related species: Eptesicus (Histiotus) macrotus and E. (H.) montanus, and their relationship with a third, E. (H.) magellanicus. The three sympatric species bear marked resemblance to each other, but can be differentiated morphologically. Furthermore, previous studies have been unable to differentiate the species from each other at a molecular level. In order to disentangle the phylogenetic relationships of these species, we examined the differentiation patterns and evolutionary history of the three Eptesicus (H.) species from Chile at the whole genome level. The nuclear DNA statistics between the species suggest strong gene flow and recent hybridization between E. (H.) montanus and E. (H.) macrotus, whereas E. (H.) magellanicus shows a higher degree of isolation. In contrast, mitochondrial DNA shows a closer relationship between E. (H.) magellanicus and E. (H.) montanus. Opposing patterns in mtDNA and nuclear markers are often due to differences in dispersal, and here it could be both as result of isolation in refugia during the last glacial maximum and female philopatry and male-biased dispersal. In conclusion, this study shows the importance of both the nuclear and mitochondrial DNA in resolving phylogenetic relationships and species histories.Understanding mechanisms involved in speciation can be challenging, especially when hybridization or introgression blurs species boundaries. In bats, resolving relationships of some closely related groups has proved difficult due subtle interspecific variation both in morphometrics and molecular data sets. The endemic South American Histiotus bats, currently considered a subgenus of Eptesicus, harbor unresolved phylogenetic relationships and of those is a trio consisting of two closely related species: Eptesicus (Histiotus) macrotus and Eptesicus (Histiotus) montanus, and their relationship with a third, Eptesicus (Histiotus) magellanicus. The three sympatric species bear marked resemblance to each other, but can be differentiated morphologically. Furthermore, previous studies have been unable to differentiate the species from each other at a molecular level. In order to disentangle the phylogenetic relationships of these species, we examined the differentiation patterns and evolutionary history of the three Eptesicus (H.) species at the whole-genome level. The nuclear DNA statistics between the species suggest strong gene flow and recent hybridization between E. (H.) montanus and E. (H.) macrotus, whereas E. (H.) magellanicus shows a higher degree of isolation. In contrast, mitochondrial DNA shows a closer relationship between E. (H.) magellanicus and E. (H.) montanus. Opposing patterns in mtDNA and nuclear markers are often due to differences in dispersal, and here it could be both as a result of isolation in refugia during the last glacial maximum and female philopatry and male-biased dispersal. In conclusion, this study shows the importance of both the nuclear and mitochondrial DNA in resolving phylogenetic relationships and species histories.Peer reviewe